EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations

Spatio-temporal patterns in electroencephalography (EEG) can be described by microstate analysis, a discrete approximation of the continuous electric field patterns produced by the cerebral cortex. Resting-state EEG microstates are largely determined by alpha frequencies (8-12 Hz) and we recently de...

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Main Authors: F. von Wegner, S. Bauer, F. Rosenow, J. Triesch, H. Laufs
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage
Subjects:
EEG
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811920308582
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spelling doaj-567899f61ee04bda9aec420b332c9ed72020-12-17T04:46:57ZengElsevierNeuroImage1095-95722021-01-01224117372EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillationsF. von Wegner0S. Bauer1F. Rosenow2J. Triesch3H. Laufs4Corresponding author at: School of Medical Sciences, University of New South Wales, Wallace Wurth Building, Kensington, NSW 2052, Australia.; School of Medical Sciences, University of New South Wales, Wallace Wurth Building, Kensington, NSW 2052, Australia; Epilepsy Center Frankfurt Rhine-Main, Center of Neurology and Neurosurgery, University Hospital Frankfurt and Center for Personalized Translational Epilepsy Research (CePTER), Goethe University Frankfurt, Frankfurt am Main, GermanyEpilepsy Center Frankfurt Rhine-Main, Center of Neurology and Neurosurgery, University Hospital Frankfurt and Center for Personalized Translational Epilepsy Research (CePTER), Goethe University Frankfurt, Frankfurt am Main, GermanyEpilepsy Center Frankfurt Rhine-Main, Center of Neurology and Neurosurgery, University Hospital Frankfurt and Center for Personalized Translational Epilepsy Research (CePTER), Goethe University Frankfurt, Frankfurt am Main, GermanyFrankfurt Institute for Advanced Studies (FIAS), Frankfurt am Main, GermanyDepartment of Neurology, Christian-Albrechts University Kiel, Arnold-Heller-Strasse 3, Kiel 24105, GermanySpatio-temporal patterns in electroencephalography (EEG) can be described by microstate analysis, a discrete approximation of the continuous electric field patterns produced by the cerebral cortex. Resting-state EEG microstates are largely determined by alpha frequencies (8-12 Hz) and we recently demonstrated that microstates occur periodically with twice the alpha frequency.To understand the origin of microstate periodicity, we analyzed the analytic amplitude and the analytic phase of resting-state alpha oscillations independently. In continuous EEG data we found rotating phase patterns organized around a small number of phase singularities which varied in number and location. The spatial rotation of phase patterns occurred with the underlying alpha frequency. Phase rotors coincided with periodic microstate motifs involving the four canonical microstate maps. The analytic amplitude showed no oscillatory behaviour and was almost static across time intervals of 1-2 alpha cycles, resulting in the global pattern of a standing wave.In n=23 healthy adults, time-lagged mutual information analysis of microstate sequences derived from amplitude and phase signals of awake eyes-closed EEG records showed that only the phase component contributed to the periodicity of microstate sequences. Phase sequences showed mutual information peaks at multiples of 50 ms and the group average had a main peak at 100 ms (10 Hz), whereas amplitude sequences had a slow and monotonous information decay. This result was confirmed by an independent approach combining temporal principal component analysis (tPCA) and autocorrelation analysis.We reproduced our observations in a generic model of EEG oscillations composed of coupled non-linear oscillators (Stuart-Landau model). Phase-amplitude dynamics similar to experimental EEG occurred when the oscillators underwent a supercritical Hopf bifurcation, a common feature of many computational models of the alpha rhythm.These findings explain our previous description of periodic microstate recurrence and its relation to the time scale of alpha oscillations. Moreover, our results corroborate the predictions of computational models and connect experimentally observed EEG patterns to properties of critical oscillator networks.http://www.sciencedirect.com/science/article/pii/S1053811920308582EEGResting-stateAlpha oscillationsMicrostatesPhase rotors
collection DOAJ
language English
format Article
sources DOAJ
author F. von Wegner
S. Bauer
F. Rosenow
J. Triesch
H. Laufs
spellingShingle F. von Wegner
S. Bauer
F. Rosenow
J. Triesch
H. Laufs
EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
NeuroImage
EEG
Resting-state
Alpha oscillations
Microstates
Phase rotors
author_facet F. von Wegner
S. Bauer
F. Rosenow
J. Triesch
H. Laufs
author_sort F. von Wegner
title EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
title_short EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
title_full EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
title_fullStr EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
title_full_unstemmed EEG microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
title_sort eeg microstate periodicity explained by rotating phase patterns of resting-state alpha oscillations
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2021-01-01
description Spatio-temporal patterns in electroencephalography (EEG) can be described by microstate analysis, a discrete approximation of the continuous electric field patterns produced by the cerebral cortex. Resting-state EEG microstates are largely determined by alpha frequencies (8-12 Hz) and we recently demonstrated that microstates occur periodically with twice the alpha frequency.To understand the origin of microstate periodicity, we analyzed the analytic amplitude and the analytic phase of resting-state alpha oscillations independently. In continuous EEG data we found rotating phase patterns organized around a small number of phase singularities which varied in number and location. The spatial rotation of phase patterns occurred with the underlying alpha frequency. Phase rotors coincided with periodic microstate motifs involving the four canonical microstate maps. The analytic amplitude showed no oscillatory behaviour and was almost static across time intervals of 1-2 alpha cycles, resulting in the global pattern of a standing wave.In n=23 healthy adults, time-lagged mutual information analysis of microstate sequences derived from amplitude and phase signals of awake eyes-closed EEG records showed that only the phase component contributed to the periodicity of microstate sequences. Phase sequences showed mutual information peaks at multiples of 50 ms and the group average had a main peak at 100 ms (10 Hz), whereas amplitude sequences had a slow and monotonous information decay. This result was confirmed by an independent approach combining temporal principal component analysis (tPCA) and autocorrelation analysis.We reproduced our observations in a generic model of EEG oscillations composed of coupled non-linear oscillators (Stuart-Landau model). Phase-amplitude dynamics similar to experimental EEG occurred when the oscillators underwent a supercritical Hopf bifurcation, a common feature of many computational models of the alpha rhythm.These findings explain our previous description of periodic microstate recurrence and its relation to the time scale of alpha oscillations. Moreover, our results corroborate the predictions of computational models and connect experimentally observed EEG patterns to properties of critical oscillator networks.
topic EEG
Resting-state
Alpha oscillations
Microstates
Phase rotors
url http://www.sciencedirect.com/science/article/pii/S1053811920308582
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